88 S EVE N Host Shifts, the Evolution of Communication, and Speciation in the Enchenopa binotata Species Complex of Treehoppers REGINALD B. COCROFT, RAFAEL L. RODRÍGUEZ, AND RANDY E. HUNT Speciation in animals is promoted by the evolution of behavioral differences that reduce attraction, mating, and fertilization between individuals in diverging populations (Mayr 1963; West-Eberhard 1983; Eberhard 1985, 1994, 1996; Coyne and Orr 2004). Behavioral traits involved in communication between the sexes often provide the most immediate contributions to reproductive isolation (Blair 1955; Claridge 1990; Ryan and Rand 1993; Bridle and Ritchie 2001; Gerhardt and Huber 2002; Kirkpatrick and Ravigné 2002). Consequently, identifying the evolutionary forces that lead to changes in sexual communication is necessary to understand the evolution of behavioral isolation and its contribution to divergence and speciation. The relationship between sexual communication and speciation depends on the extent of interactions between individuals from the diverging populations. When geography and/or ecology prevent such interactions during the speciation process, differences in mating signals and preferences may become important upon secondary contact, at which point the differences may be enhanced by selection against hybridization (Howard 1993; Kelly and Noor 1996; Coyne and Orr 1997; Jiggins and Mallet 2000; Servedio and Noor 2003). In contrast, when the geography and ecology of speciation do lead to interactions between individuals from the diverging populations (i.e., when speciation occurs in sympatry ), behavioral causes of reproductive isolation are important from the outset (Kondrashov et al. 1998; Kondrashov and Kondrashov 1999; Kirkpatrick and Ravigné 2002). Sympatric speciation is implicated in the diversiﬁcation of host-speciﬁc, plant-feeding insects (Mallet 2001; Berlocher and Feder 2002; Bush and Butlin 2004). In these insects, which comprise a large fraction of animal diversity (Price 2002; Bush and Butlin 2004), speciation is often associated with changes in host-plant use. Host shifts have widespread consequences for life-history traits, and aspects of insect adaptation to their host plants can lead to assortative mating as a pleiotropic effect (Wood and Keese 1990; Craig et al. 1993; Wood 1993; Feder 1998; Berlocher and Feder 2002; see also Jiggins et al. 2005). Colonization of a new host environment may also have a profound inﬂuence on the evolution of communication. In this chapter we examine the role of communication systems in the diversiﬁcation of the Enchenopa binotata species complex of treehoppers (Hemiptera: Membracidae), a clade of 11 sap-feeding species distributed across eastern North America. Based on the career-long series of studies by T. K. Wood and colleagues, this group provides one of the most widely cited examples of sympatric speciation in plant-feeding insects (Tauber and Tauber 1989; Wood 1993; Berlocher and Feder 2002; Coyne and Orr 2004). The E. binotata complex is especially promising for studies of the relationship between host shifts and behavioral isolation (Landolt and Phillips 1997; Etges 2002), because of the rich understanding of its natural history, comparative biology, and communication behavior. We ﬁrst discuss the role of ecological factors in promoting assortative mating among populations of E. binotata on ancestral and novel species of host plant. We then examine the role of sexual communication in behavioral isolation among E. binotata species in the present. We explore sources of divergent sexual and natural selection that could alter the evolutionary trajectory of mating signals and preferences after a host shift. We also consider ways in which developmental inﬂuences on sexual communication may affect gene ﬂow between populations on ancestral and novel hosts (before any evolutionary change in communication systems has occurred), and how developmental plasticity may generate changes in sexual selection regimes. We will argue that for plant-feeding insects, sexual communication systems provide an important link between host use, assortative mating, and divergent HOST SHIFTS, THE EVOLUTION OF COMMUNICATION, AND SPECIATION 89 selection and may be a key component of sympatric speciation through host shifts. Ecological Isolation in the E. binotata Complex Thomas K. Wood and colleagues developed the E. binotata complex as a model for evaluating the role of host shifts in promoting genetic divergence in sympatry (Wood and Guttman 1983; Wood 1993). (A complete list of Wood’s publications is provided by Deitz and Bartlett [2004].) The central message of this research is that successful colonization of a novel host can lead to immediate assortative mating between populations on the original and novel hosts, facilitating a response to divergent selection imposed by differences between the host species. The most immediate factor contributing to assortative mating after a host shift...

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